Department Fish Ecology and Evolution

Fish Genomics

Fascinated by the diversity of fish, this group aims to understand processes and factors creating variation and differentiation at the genomic level.

We analyse large-scale genomic data sets to gain a better understanding how processes like selection, drift, mutation, and recombination act in concert to create the observed genomic patterns of varying diversity and divergence along the genome. To achieve this aim we combine population genetics, bioinformatics, and an understanding of the study organisms (mainly fish).

Selected publications

A European whitefish linkage map and its implications for understanding genome-wide synteny between salmonids following whole genome duplication

Genomic datasets continue to increase in number due to the ease of production for a wider selection of species including non-model organisms. For many of these species, especially those with large or polyploid genomes, highly contiguous and well-annotated genomes are still rare due to the complexity and cost involved in their assembly. As a result, a common starting point for genomic work in non-model species is the production of a linkage map. Dense linkage maps facilitate the analysis of genomic data in a variety of ways, from broad scale observations regarding genome structure e.g. chromosome number and type or sex-related structural differences, to fine scale patterns e.g. recombination rate variation and co-localization of differentiated regions. Here we present both sex-averaged and sex-specific linkage maps for Coregonus sp. "Albock", a member of the European whitefish lineage (C. lavaretus spp. complex), containing 5395 single nucleotide polymorphism (SNP) loci across 40 linkage groups to facilitate future investigation into the genomic basis of whitefish adaptation and speciation. The map was produced using restriction-site associated digestion (RAD) sequencing data from two wild-caught parents and 156 F1 offspring. We discuss the differences between our sex-averaged and sex-specific maps and identify genome-wide synteny between C. sp. "Albock" and Atlantic Salmon (Salmo salar), which have diverged following the salmonid-specific whole genome duplication. Our analysis confirms that many patterns of synteny observed between Atlantic Salmon and Oncorhynchus and Salvelinus species are also shared by members of the Coregoninae subfamily. We also show that regions known for their species-specific rediploidization history can pose challenges for synteny identification since these regions have diverged independently in each salmonid species following the salmonid-specific whole genome duplication. The European whitefish map provided here will enable future studies to understand the distribution of loci of interest, e.g. FST outliers, along the whitefish genome as well as assisting with the de novo assembly of a whitefish reference genome.

Population size changes and selection drive patterns of parallel evolution in a host–virus system

Predicting the repeatability of evolution remains elusive. Theory and empirical studies suggestthat strong selection and large population sizes increase the probability for parallelevolution at the phenotypic and genotypic levels. However, selection and population sizes arenot constant, but rather change continuously and directly affect each other even on shorttime scales. Here, we examine the degree of parallel evolution shaped through ecoevolutionarydynamics in an algal host population coevolving with a virus. We find highdegrees of parallelism at the level of population size changes (ecology) and at the phenotypiclevel between replicated populations. At the genomic level, we find evidence for parallelism,as the same large genomic region was duplicated in all replicated populations, but alsosubstantial novel sequence divergence between replicates. These patterns of genome evolutioncan be explained by considering population size changes as an important driver of rapidevolution.

A dense linkage map of Lake Victoria cichlids improved the Pundamilia genome assembly and revealed a major QTL for sex-determination

Genetic linkage maps are essential for comparative genomics, high quality genome sequence assembly and fine scale quantitative trait locus (QTL) mapping. In the present study we identified and genotyped markers via restriction-site associated DNA (RAD) sequencing and constructed a genetic linkage map based on 1,597 SNP markers of an interspecific F2 cross of two closely related Lake Victoria cichlids (Pundamilia pundamilia and P. sp. 'red head'). The SNP markers were distributed on 22 linkage groups and the total map size was 1,594 cM with an average marker distance of 1.01 cM. This high-resolution genetic linkage map was used to anchor the scaffolds of the Pundamilia genome and estimate recombination rates along the genome. Via QTL mapping we identified a major QTL for sex in a ∼1.9 Mb region on Pun-LG10, which is homologous to Oreochromis niloticus LG 23 (Ore-LG23) and includes a well-known vertebrate sex-determination gene (amh).

Variation in recombination frequency and distribution across eukaryotes: patterns and processes

Recombination, the exchange of DNA between maternal and paternal chromosomes during meiosis, is an essential feature of sexual reproduction in nearly all multicellular organisms. While the role of recombination in the evolution of sex has received theoretical and empirical attention, less is known about how recombination rate itself evolves and what influence this has on evolutionary processes within sexually reproducing organisms. Here, we explore the patterns of, and processes governing recombination in eukaryotes. We summarize patterns of variation, integrating current knowledge with an analysis of linkage map data in 353 organisms. We then discuss proximate and ultimate processes governing recombination rate variation and consider how these influence evolutionary processes. Genome-wide recombination rates (cM/Mb) can vary more than tenfold across eukaryotes, and there is large variation in the distribution of recombination events across closely related taxa, populations and individuals. We discuss how variation in rate and distribution relates to genome architecture, genetic and epigenetic mechanisms, sex, environmental perturbations and variable selective pressures. There has been great progress in determining the molecular mechanisms governing recombination, and with the continued development of new modelling and empirical approaches, there is now also great opportunity to further our understanding of how and why recombination rate varies. This article is part of the themed issue 'Evolutionary causes and consequences of recombination rate variation in sexual organisms'.

The observation of habitat-specific phenotypes suggests the action of natural selection. The three-spined stickleback (Gasterosteus aculeatus) has repeatedly colonized and adapted to diverse freshwater habitats across the northern hemisphere since the last glaciation, while giving rise to recurring phenotypes associated with specific habitats. Parapatric lake and river populations of sticklebacks harbour distinct parasite communities, a factor proposed to contribute to adaptive differentiation between these ecotypes. However, little is known about the transcriptional response to the distinct parasite pressure of those fish in a natural setting. Here, we sampled wild-caught sticklebacks across four geographical locations from lake and river habitats differing in their parasite load. We compared gene expression profiles between lake and river populations using 77 whole-transcriptome libraries from two immune-relevant tissues, the head kidney and the spleen. Differential expression analyses revealed 139 genes with habitat-specific expression patterns across the sampled population pairs. Among the 139 differentially expressed genes, eight are annotated with an immune function and 42 have been identified as differentially expressed in previous experimental studies in which fish have been immune challenged. Together, these findings reinforce the hypothesis that parasites contribute to adaptation of sticklebacks in lake and river habitats.

Genomics of divergence along a continuum of parapatric population differentiation

The patterns of genomic divergence during ecological speciation are shaped by a combination of evolutionary forces. Processes such as genetic drift, local reduction of gene flow around genes causing reproductive isolation, hitchhiking around selected variants, variation in recombination and mutation rates are all factors that can contribute to the heterogeneity of genomic divergence. On the basis of 60 fully sequenced three-spined stickleback genomes, we explore these different mechanisms explaining the heterogeneity of genomic divergence across five parapatric lake and river population pairs varying in their degree of genetic differentiation. We find that divergent regions of the genome are mostly specific for each population pair, while their size and abundance are not correlated with the extent of genome-wide population differentiation. In each pair-wise comparison, an analysis of allele frequency spectra reveals that 25–55% of the divergent regions are consistent with a local restriction of gene flow. Another large proportion of divergent regions (38–75%) appears to be mainly shaped by hitchhiking effects around positively selected variants. We provide empirical evidence that alternative mechanisms determining the evolution of genomic patterns of divergence are not mutually exclusive, but rather act in concert to shape the genome during population differentiation, a first necessary step towards ecological speciation.

Extensive copy-number variation of young genes across stickleback populations

Duplicate genes emerge as copy-number variations (CNVs) at the population level, and remain copy-number polymorphic until they are fixed or lost. The successful establishment of such structural polymorphisms in the genome plays an important role in evolution by promoting genetic diversity, complexity and innovation. To characterize the early evolutionary stages of duplicate genes and their potential adaptive benefits, we combine comparative genomics with population genomics analyses to evaluate the distribution and impact of CNVs across natural populations of an eco-genomic model, the three-spined stickleback. With whole genome sequences of 66 individuals from populations inhabiting three distinct habitats, we find that CNVs generally occur at low frequencies and are often only found in one of the 11 populations surveyed. A subset of CNVs, however, displays copy-number differentiation between populations, showing elevated within-population frequencies consistent with local adaptation. By comparing teleost genomes to identify lineage-specific genes and duplications in sticklebacks, we highlight rampant gene content differences among individuals in which over 30% of young duplicate genes are CNVs. These CNV genes are evolving rapidly at the molecular level and are enriched with functional categories associated with environmental interactions, depicting the dynamic early copy-number polymorphic stage of genes during population differentiation.

Terminated projects

Stickleback Speciation Genomics

In this on-going large-scale genomics project we study the genome evolution at a population scale in an ecological and evolutionary model species, the three-spined stickleback. We analyse whole genome data from 66 three-spined sticklebacks, which originate from three ecotypes, a marine population and multiple lake-river population pairs, over a broad geographical range. Population diversity is contrasted between parapatric and geographically distant (allopatric) population pairs undergoing parallel ecological Adaptation.

Contact

Collaboration

Publications

Genomics of divergence along a continuum of parapatric population differentiation

The patterns of genomic divergence during ecological speciation are shaped by a combination of evolutionary forces. Processes such as genetic drift, local reduction of gene flow around genes causing reproductive isolation, hitchhiking around selected variants, variation in recombination and mutation rates are all factors that can contribute to the heterogeneity of genomic divergence. On the basis of 60 fully sequenced three-spined stickleback genomes, we explore these different mechanisms explaining the heterogeneity of genomic divergence across five parapatric lake and river population pairs varying in their degree of genetic differentiation. We find that divergent regions of the genome are mostly specific for each population pair, while their size and abundance are not correlated with the extent of genome-wide population differentiation. In each pair-wise comparison, an analysis of allele frequency spectra reveals that 25–55% of the divergent regions are consistent with a local restriction of gene flow. Another large proportion of divergent regions (38–75%) appears to be mainly shaped by hitchhiking effects around positively selected variants. We provide empirical evidence that alternative mechanisms determining the evolution of genomic patterns of divergence are not mutually exclusive, but rather act in concert to shape the genome during population differentiation, a first necessary step towards ecological speciation.

Extensive copy-number variation of young genes across stickleback populations

Duplicate genes emerge as copy-number variations (CNVs) at the population level, and remain copy-number polymorphic until they are fixed or lost. The successful establishment of such structural polymorphisms in the genome plays an important role in evolution by promoting genetic diversity, complexity and innovation. To characterize the early evolutionary stages of duplicate genes and their potential adaptive benefits, we combine comparative genomics with population genomics analyses to evaluate the distribution and impact of CNVs across natural populations of an eco-genomic model, the three-spined stickleback. With whole genome sequences of 66 individuals from populations inhabiting three distinct habitats, we find that CNVs generally occur at low frequencies and are often only found in one of the 11 populations surveyed. A subset of CNVs, however, displays copy-number differentiation between populations, showing elevated within-population frequencies consistent with local adaptation. By comparing teleost genomes to identify lineage-specific genes and duplications in sticklebacks, we highlight rampant gene content differences among individuals in which over 30% of young duplicate genes are CNVs. These CNV genes are evolving rapidly at the molecular level and are enriched with functional categories associated with environmental interactions, depicting the dynamic early copy-number polymorphic stage of genes during population differentiation.

Adaptive Introgression in Soay Sheep

Admixture, the mixing between divergent genomes, is widely thought to hinder local adaptation. However, a handful of recent studies have suggested that admixture can promote local adaptation. The Soay sheep of St Kilda are a primitive breed that have been the subject of a well documented long-term study, where data on life history, morphology, parasite burden, and pedigree information have been collected for over 7000 sheep. We followed up historical anecdotal evidence of an admixture event in the mid-late 1800s by screening 486 Soay sheep on a 50k ovine SNP chip. We found evidence for such a recent admixture event with a more modern, domesticated breed in the analysed genomic data. Utilising the HapMap dataset of over 60 different sheep breeds we showed that several haplotypes, previously demonstrated to be under selection in this population, have been introduced into Soay sheep from more modern breeds. Our study demonstrates that the introgression of domesticated alleles into wild populations is not necessarily disadvantageous and in fact it may provide a novel source of genetic variation capable of generating rapid evolutionary changes.

Project partners

Adaptive Radiation of African Mormyrids

In this project we build a first comprehensive phylogeny of the mormyrid genus Campylomormyrus. We further assessed the importance of two very unusual features of these peculiar fish for the speciation process: their trunk-like elongated snout and their ability to produce electric signals for orientation and communication. Using morphometrics we demonstrated that the trunk morphology correlates with reproductively isolated groups characterised by specific electric signals, i.e. species. Behavioural studies further indicated that the waveform of the Electric Organ Discharge (EOD) causes assortative mating and therefore reproductive isolation. Because the EOD is also used for electrolocation of prey, we proposed the EOD as a ‘magic trait’ promoting the ecological speciation of Campylomormyrus within the Congo River.